Trophodynamics of the Antarctic toothfish (Dissostichus mawsoni) in the Antarctic Peninsula: Ontogenetic changes in diet composition and prey fatty acid profiles

The Antarctic toothfish (Dissostichus mawsoni) is the largest notothenioid species in the Southern Ocean, playing a keystone role in the trophic web as a food source for marine mammals and a top predator in deep-sea ecosystems. Most ecological knowledge on this species relies on samples from areas where direct fishing is allowed, whereas in areas closed to fishing, such as the Antarctic Peninsula (AP), there are still key ecological gaps to ensure effective conservation, especially regarding our understanding of its trophic relationships within the ecosystem. Here, we present the first comprehensive study of the feeding behavior of Antarctic toothfish caught in the northern tip of the AP, during two consecutive fishing seasons (2019/20 and 2020/21). Stomach content was analyzed according to size-classes, sex and season. Macroscopic morphological analysis was used to identify prey, whereas DNA analysis was used in highly digested prey items. Fatty acid analysis was conducted to determine the prey’s nutritional composition. The diet mainly consisted of Macrouridae, Cephalopoda, Anotopteridae, and Channichthyidae. Other prey items found were crustaceans and penguin remains; however, these were rare in terms of their presence in stomach samples. Sex had no effect on diet, whereas size-class and fishing season influenced prey composition. From 27 fatty acid profiles identified, we observed two different prey groups of fishes (integrated by families Anotopteridae, Macrouridae and Channichthyidae) and cephalopods. Our results revealed a narrow range of prey items typical of a generalist predator, which probably consumes the most abundant prey. Understanding the diet and trophic relationships of Antarctic toothfish is critical for a better comprehension of its role in the benthic-demersal ecosystem of the AP, key for ecosystemic fisheries management, and relevant for understanding and predicting the effect of climate change on this species.

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Introduction
The Southern Ocean is characterized by extreme physical conditions that have shaped a unique, endemic and highly adapted fauna [1,2].A good example is its fish fauna, characterized by relatively low species richness and diversity, highly dominated by the suborder Notothenioidei, a group highly adapted to cold waters [1,3].Among this group, Dissostichus mawsoni commonly known as Antarctic toothfish (hereafter TOA) is a species circumpolar distributed above 60°S latitude, at water depths up to 3000 meters along the shelf and continental slope, with temperatures below 0°C [4][5][6].Individuals can exceed 2 meters length and 100 kg weight [7,8], lasting over 30 years with a first sexual maturation between 12 and 16 years of age [5,9].By far is the larger fish species, playing a key ecological role in the trophic web, both as food source for marine mammals such as cetaceans [10] and seals [11], and as the top predator in deep-sea ecosystems, structuring the size and population dynamics of its prey species through a trophic cascade [8,12].
TOA is a valuable fishing resource targeted by an international bottom-set longline fleet which is managed by the Commission for the Conservation of Antarctic Marine Living Resources (CCAMLR), whose main objective is to achieve a balance between the rational use and conservation of fishing stocks.CCAMLR also promotes ecosystem-based fisheries management, through conservation measures based on exploitation levels that ensure recruitment stability and ecological relationships functioning to avoid irreversible changes in the marine ecosystems [13].At present, TOA is targeted throughout almost their entire distribution range, with a total annual catch of around 4000 tons occurring mostly in the Ross Sea, East Antarctica and the Weddell Sea [14].The only exception is the Antarctic Peninsula (AP, FAO Statistical Subarea 48.1), where direct fishing for notothenioids is prohibited, due to population collapses after overexploitation in the 1970s and 1980s and still no evidence of population recovery [15].Nowadays, CCAMLR only allows exploratory fisheries with minimum catch limits aimed to obtain information on the biological and ecological interspecific information for ecosystem-based purposes [8,[16][17][18].
Prohibition of regular fishing activities has determined gaps of knowledge regarding the population and community dynamics of the TOA in Subarea 48.1, thus CCAMLR Scientific Committee has asked for new studies to reduce uncertainty [19].Information of trophic dynamics is scarce, and diet analysis based on prey composition is necessary to understand population dynamics and its interaction with the surrounding community [18].Macroscopic morphological analysis of stomach contents is a widely used technique for prey identification.Despite limitations associated with fast digestion of some prey item that could be just representative of short-term feeding [20] as it can provide information on intra-and interspecific relationships.Across the SO, where fisheries regularly occurs, several dietary studies have been conducted using macroscopic and molecular prey identification [8,21] with recent studies using a combination of both, providing new information that have improved the understanding of its trophic ecology [22].This type of approach complemented with other methods such as fatty acid analyses (lipids as biomarkers) have proven to be a powerful tools to infer trophic interactions and obtain longer-term information on energy flow through the ecosystem [22][23][24][25].
Feeding patterns described from TOA stomachs using both macroscopical prey composition and fatty acid profiles [23,24] have indicated that this species is an opportunistic predator, whose diet depends on the availability of prey in a given hábitat [16,26].Based on this, current scientific consensus supports the idea of TOA as a generalist predator [19], whose diet composition varies ontogenetically, due to changes in vertical distribution throughout its life history [8,27].
Understanding the feeding ecology of Antarctic toothfish on the Antarctic Peninsula is crucial to assess its ecological role, key for the ecosystem-based fishery management to avoid adverse indirect effects.A research program conducted by Ukraine in Subarea 48.1 allow us to analyze stomachs collected over two consecutive summer seasons (2020 and 2021), and thus we did the first comprehensive study of feeding ecology through stomach content and fatty acid analyses.Here, we identified prey composition of TOA in the AP using macroscopic guides and DNA for digested prey, tested the effect of size-class length, fishing season and sex on diet variability, and characterized nutritional prey contribution from fatty acid profiles.We hypothesized that the diet composition changes with size-class length, showing an ontogenetic change in feeding habits.).Squid pieces were used as bait, not considered in subsequent stomach content analysis.Each individual TOA was weighted (gr), sexed and total length (cm) recorded onboard.Extracted stomachs were stored frozen at -20°C and sent for analysis to the Bioresources Laboratory of the Chilean Antarctic Institute (INACH) in Punta Arenas, Chile.

Stomach content analysis
Whole stomachs were thawed and content was weighed (mST) to the nearest 0.01 g using an electronic scale.Examination of prey included records of digestion status, taxonomic identification, wet weight (gr), length (cm) and fatty acid composition.
Digestion status was noted using a five-point scale: not digested, slightly digested, moderately digested, advanced digested and heavily digested.Identification was to the lowest taxonomic level through macroscopic morphological analysis (mid) using identification keys [4,28].Moderately to advanced digested prey were identified using genetic procedures (gid).Tissue samples from dorsal muscle were collected (∼10 mg) and stored in ethanol (90%) at -20°C.DNA extraction was performed with 0,150 g of tissue using DNeasy® PowerSoil® Pro (Cat.:47016)following the manufacturer's protocol.Each sample was quantified using NanoQuant microplate Infinite M200pro.To amplify the mitochondrial 16s gene, primers were synthesized and purified by HPLC at Macrogen (Korea), using the sequence described by Berry et al. (2015) (forward: 5'-CGAGAAGACCCTRTGGAGCT-3' and reverse: 5'-GGATWGCGCTGTTATCCCT-3').PCR was performed using Invitrogen TM Platinum TM SuperFi TM II DNA Polymerase and the following thermocycling cycle: initial denaturation at 98°C for 5 min, 35 cycles of initial denaturation at 98°C for 10 s, annealing at 56°C for 5 s, extension at 72°C for 45 s, and a final extension at 72°C for 5 min.Each PCR product was run on a TBE 1,8 % agarose gel and purified using the UltraClean® 15 DNA Purification Kit (Cat.:12100-300),following the manufacturer's protocol.The purified PCR products were quantified and DNA sequencing was conducted in Macrogen using forward and reverse primers.The sequences obtained were joined and analyzed using the CLC Main Workbench (version 8.0).Taxonomic identification was performed using the NCBI database using a degree of similarity between the obtained sequences and reference sequences higher than 99%.
For fatty acid analysis, ten grams of prey muscle tissue was stored in 15 ml falcon tubes, frozen at -20° C and lyophilized.Samples were analyzed at the Nutrition Laboratory of the Department of Agricultural and Aquaculture Sciences of the Universidad de Magallanes (Punta Arenas, Chile).Qualitative and quantitative determination of fatty acids was carried out by transforming them into methyl esters (FAMES) and subjected to gas chromatographic analysis.Total lipids from the sample were estimated following the methodology proposed by [28] and then the fatty acids present in the sample were analyzed according to the methodology described by [29].
Extracted lipids were deposited in a 50 ml capacity balloon, to which 4 ml of methanolic solution of 0.5N sodium hydroxide were immediately added.The oxygen was then displaced from the balloon with a stream of nitrogen, refluxed in a batch with boiling water for 10 min and 5 ml of 14% Boron Trifluoride (BF3-CH3OH, Sigma-Aldrich) was added to recirculation for 30 min.Then 2 ml of hexane was added and almost immediately 20 ml of saturated sodium chloride (NaCl) was added and shaken vigorously for 15 sec.Saturated NaCl was added again up to the neck of the balloon, allowed to cool to room temperature and finally, with a Pasteur pipette, the upper layer containing the methyl esters was extracted to be transferred to a vial for chromatography.
For gas chromatography analysis, an Agilent 7890B gas chromatograph equipped with an autosampler and FID detector was used.In addition, a HP-88 high polarity column (60 m x 0.20 µm x 0.25 mm) was used.The carrier gas (H2) flow rate was 1 ml/min and the flow split injection system with a 50:1 vent ratio was used.The injector temperature was 250 °C and the detector temperature was 280°C.The oven temperature program was 120°C for 5 min, with a ramp of 3°C/min up to 220°C (5 min).The injection volume was 1 µl and a blank was performed every other analysis.All transesterification was performed in duplicate.Abbreviated notations of the form A:B (n-x) were used, where A represents the number of carbon atoms, B the number of double bonds and x gives the position of the first double bond counting from the terminal methyl group.The concentration of each fatty acid was expressed as the relative percentage of the total fatty acid content (% FAs) ± standard deviation.

Indicators of diet composition
The diet was analyzed only in samples with stomach contents, excluding empty stomachs.
Diet composition and the importance of each prey item was calculated according the percentage of frequency of occurrence (F%), weight (M%) and number (N%), respectively expressed as: Ai is the number of individuals that consumed prey i and A is the total number of stomachs examined.Mi corresponds to the total wet weight of the prey i and Mt is the total wet weight of the prey.Ni is the total number of prey i and Nt the total number of prey.
From these indicators, the importance of each type of prey within the diet was calculated using the index of relative importance (IRI) [30], expressed as: For a better interpretation of the relative contribution of each dam, we calculated the relative importance index as a percentage (IRI%) [31], expressed as: • 100 In order to analyze diet among predator length, the IRI% was calculated into three size-class groups, G1: <100 cm, G2: 100-140 cm and G3: 140-180 cm.
Feeding intensity was evaluated according the repletion index (RI) [32], expressed as: Where mST is the weight of the stomach contents and mDM is the total weight of the individual.

Statistical analysis
A multivariate generalized linear model (MGLM) was used to test variability in the prey specific numeric abundance (N) according sex, fishing season and size-class.MGLM provides a multivariate test for the former factors and a univariate test for each prey item.
The lowest Akaike's information criterion (AIC) was selected to identify the model that best explained the amount of variation in N. MGLM was run with Poisson distribution and 999 Monte-Carlo permutations using mvabund v.4.2.1 R package [33].To graphically visualize variability among factors, a non-metric multidimensional scaling ordination (nMDS) plot based on Bray-Curtis distances was run using vegan v.2.6-4 R package [34].
Differences in the repletion index were assessed between sex, fishing season and size-class, using sqrt function in a one-way analysis of variance (ANOVA).
A permutational analysis of variance (PERMANOVA) test, based on Bray-Curtis distance matrix was used to assess for differences among FAs composition of prey composition.A similarity percentage analysis (SIMPER) was also used to identify the fatty acids contributing most to differences between prey items and a nMDS plot was used to graphically illustrate observed patterns.
All statistical analyses were performed using Rstudio 2022.12.0+353.Map was drawn using ArcGIS 10.8.

Results
TOA individuals sampled in 2020 ranged from 64 to 174 cm TL (mean 125.
The MGLM showed that the prey specific numeric abundance was best explained by the additive (non-interaction) effect, where size-class and fishing season showed significant effect (Table 2).Sex was discarded during the AIC selection process as it had no effect (S2 Table ).As seen in the nMDS plot, diet variability was higher in G2 and G3 size groups than for G1 (Fig 4).Among identified prey, a significant effect of size-class was recorded on cephalopod consumption (Table 2) that was slightly present in groups G2 and G3 in 2020, being more relevant in 2021, especially G1 exceeding 55.0% IRI (Fig 5).On the other hand, a significant effect of the fishing season was found on Anotopteridae consumption (Table 2), which dominated G1 in 2020 (67.65% IRI) and was absent in 2021 (Fig 5).Although no significant effect of size group on other species was found, it can be seen that Macrouridae was less present in group G1 (29.99% IIR in 2020), but dominated the diet of groups G2 and G3 with 74.44% to 66.86% IRI, respectively, and Channichthyidae were particularly important to G1 in 2021 (28.87%IRI) (Fig 5) Feeding intensity was low (Repletion Index = 1.23% ± 1.42 SD) with no significant differences between fishing season (ANOVA, F(1, 154) = 0.0004 p = 0.994), sex (ANOVA, F(1, 154) = 0.057 , p= 0.812) and size classes (ANOVA, F(2, 153) = 0.102 p = 0.902).

Discussion
The present study provides the first comprehensive description of the feeding behavior of the Antarctic toothfish by combining stomach content identification with fatty acid analysis, providing a wider understanding of the feeding ecology and role of TOA in the Antarctic Peninsula.Trophic dynamics is a prerequisite for ecosystem-based fisheries management and necessary to assess potential fishing impacts on target species, which is especially true in the Antarctic Peninsula where direct fishing for notothenioids has been prohibited.

Feeding behavior
In the Antarctic Peninsula, TOA feed mainly on fishes, a prey of high nutritional value and often the most available, being usually the most important prey item for top predators in Antarctica [26,35].Macrouridae was the most important prey, similar to what has been described in previous studies from other regions, where Macrourus whitsoni and Macrourus caml, a sympatric species inhabiting the same depth range with TOA (900 and 1900 m depth), appears frequently in TOA diet and as bycatch in the fishery [5,8,17,24,26,[36][37][38].
Considering that the TOA diet is dominated by locally abundant fish species [5,39] and according to the high contribution of Macrouridae in the TOA diet observed in this study, we can assume that this group is probably the most abundant fish in the AP.Although there are no direct biomass estimations for Macrouridae in the AP, previous evidence showed this group as the most widespread representative of bycatch in 2020 and 2021 [40].
Channichthyidae was also an important prey.We identified Chionobathyscus dewitti, a species reported as one of the main prey of TOA in the Lazarev Sea and the Ross Sea [5,36], and commonly found between 600 to 1600 m depth in the Antarctic Peninsula [41,42], and over 2000 m depth in the Weddell Sea [42,43].From the fishery data, Channichthyidae is the second most abundant bycatch group in the Antarctic Peninsula [40].
Surprisingly, we observed a very low contribution of Nototheniidae, even in individuals <100 cm, where it can reach up to 35% of the diet in individuals from East Antarctica [8].It is possible that for greater energy efficiency, individuals prey on a smaller number of larger and heavier Macrouridae individuals, rather than a larger number of smaller and lighter Nototheniidae [8].Another explanation could be that the fish community in the AP is heavily dominated by Macrouridae, with reduced availability of Nototheniidae as a consequence of the population collapse in past decades [15].Although, there was an important amount of highly digested unidentified fish prey (which reached up to 60% IRI) where Nototheniidae could be present.Having said that, the reduced presence of Notheniidae was also observed in the fishery with low bycatch estimates in the area [40].
Although relatively rare, benthic crustaceans such as Nematocarcinus lanceopes and Eurythenes gryllus were also found.Both species has been recorded at depths between 500 and 2031 m [44,45], whereas E. gryllus has been reported between 550 to 7800 m depth [46,47], overlapping with TOA depth range.Another less important item was penguin remains (found in two stomachs), suggesting that part of the diet may have come from carrion.Also we found coral and rock fragments, which is indicative of benthic foraging habits [8,17,26].
The former prey composition are representative of benthopelagic fauna [4,42], confirming TOA as a demersal feeder whose feeding preferences would be restricted to the abundance of different prey [5,8,17].Also, the presence of Anotopterus vorax has been previously related to a migration to shallow waters [26].All this information confirms TOA as a top predator capable of impacting and controlling the bentho-pelagic ecosystem in the Antarctic Peninsula.
A positive correlation was observed between the TOA size and prey size, with prey size increasing as predator size increases.This is common as predator-prey interactions often depend on body size, due to the morphological limitations of the predator in agreement with the morphological ontogenetic changes in the feeding apparatus [48,49].In other diet studies, TOA subadults show a diet composed of a variety of smaller prey such as smaller fishes and benthic crustaceans, while adult individuals preyed mostly on larger demersal fishes such as Macrouridae [17].One point of variability was the presence of Anotopteridae, which although exaggerated in length, can generally be considered small prey, impacting this predator-prey relationship.
Differences in diet composition were found between size groups, with dietary variability being greater in adults (>100 cm) than in juveniles (<100 cm).This can be related to changes in buoyancy and depth range distribution [27].It is known that juveniles of TOA has a negative buoyancy, constraining depth range to shallower waters and benthic habitats, while adults have neutral buoyancy, being capable to move across a wider depth range from shallow to deep waters [4,6,17,27].This adaptation would allow TOA to avoid predators and generate changes in accessibility to different prey items.Some prey such as Cephalopoda and Channichthyidae have benthic-pelagic habits [42,50] thus being important for juveniles.On the other hand, prey such as Macrouridae are abundant in deep waters [37] becoming more important for TOA adults.Other studies have also found changes in diet with predator length [5,8,17,51], which could demonstrate that there are ontogenetic changes in the diet of Antarctic toothfish.However, because all fishes caught in this study took place deeper than 900 m depth, juveniles were not represented and the smallest individuals analyzed were 80 cm, hence, it is necessary to extend to smaller sizes probably on shallow waters to obtain more determinant results.
Other sources of variability in TOA diet have been attributed to different areas and depth strata [8,22], but interannual variability is rarely analyzed.Considering that the TOA diet can strongly reflect local fish assemblages [39], it is interesting the changes in prey composition between two consecutive fishing seasons observed in this study.In Antarctica, demersal fish assemblages can vary according to water temperatura [52], however this was not assessed in this study.The ongoing oceanographic changes well-described along the Antarctic Peninsula [53], could also be impacting the deep-water fish assemblage, hence it is important to measure physical factors to assess if they are driving changes in the distribution of prey in the area.

Fatty acids prey composition
Overall, PUFA was twice as numerous as MUFA and SAFA in all analyzed prey, which is typical in high latitude ecosystems than those from tropical [54].We also observed higher content of w3 than w6 (high w3/w6 ratio), characteristic of marine ecosystems [55].
Fish and cephalopod prey showed similar amounts of saturated fatty acids (SAFAs), mostly dominated by palmític acid (C16:0), one of the most common FAs in marine organisms, key to providing metabolic energy during growth and spawning [56].Among MUFAs there were higher values in fishes rather than cephalopods, especially oleic acid (C18:1), a fatty acid commonly found in prey that live at great depths [57,58].Both fishes and cephalopods were prey rich in PUFAs eicosapentaenoic (C20:5) and docosahexaenoic (C22:6), often considered essentials acids as most aquatic animals are not capable of synthesizing and are essential nutrient precursor, indicative of optimal animal health [56,59].According to results, TOA feeds on prey with a high proportion of MUFAs and PUFAs, where both fishes and cephalopods can supply similar amounts of energy, so there could be no need of a specialist behavior, and potentially explaining the generalist strategy commonly associated with TOA feeding.Other predators tend to have a selective behavior as the differential energetic contribution among different prey [60].Since we were not able to analyze predator tissues we could not compare the fatty acid signatures among the predator and their prey; this would have provided us with important information of quantitative trophic predator-prey relationship [61].However, the information provided here still constitutes a key information to understand energy flow and carbon transfer pathways in relation to the role of TOA in the benthic-demersal ecosystem of the Antarctic Peninsula.

Management consideration
Antarctic toothfish has been consistently managed by the CCAMLR as a key component in the food web dynamics of the Antarctic ecosystem [5,23], however, issues including the population status, ecosystem impacts of the fisheries are still to be well understood [62].
Moreover, climate change projections suggest that warming will negatively affect toothfish and other benthopelagic dwelling species [63].For this reason, a complete understanding of feeding dynamics and trophic connections is relevant for ecosystem-based stock management in order to develop fishing activities while maintaining ecosystem structure and functioning.
One risk in the toothfish fishery is the predation release, where fishing-induced changes in predator-prey relationship may generate the unbalanced proliferation of one species, destabilizing the structure and function of the food-web [22].This process could be of particular concern in environments already modified by overexploitation, such as the Antarctic Peninsula, where it is unknown how TOA and the surrounding community will respond to fishing pressure, also considering the impacts of climate change in the area.
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Stomach contents of 159 TOA individuals were analyzed from catches made by the Ukrainian commercial vessel Calipso in Subarea 48.1 (northern tip of the Antarctic Peninsula, Fig 1).Fishing operations were carried out in February 2020 (n = 89 stomachs) and February 2021 (n = 70 stomachs) using spanish bottom longlines at depths between 924-1560 meters in 2020 and between 1075-1371 meters in 2021 (S1 Table

Fig 1 .
Fig 1. Locations of the fishing hauls carried out in the northern tip of the Antarctic Peninsula

Fig 2 .
Fig 2. Size structure of Dissostichus mawsoni individuals caught in the northern tip of the

Fig 3 .
Fig 3. Size structure of prey items and its relationship with Dissostichus mawsoni individuals

Table 1 .
Diet composition of Dissostichus mawsoni in the northern tip of the Antarctic

Table 2 .
Results of MGLM testing effect of size-class and fishing season on the prey specific numeric abundance in the stomachs of the Antarctic toothfish in the northern tip of the

Table 3 .
Fatty acid (FA) composition (% of total FA, mean ± se) of prey items in the Dissostichus mawsoni diet from individuals collected in the northern tip of the Antarctic Peninsula.(SAFA are saturated fatty acids, MUFA are monounsaturated fatty acids and PUFA are polyunsaturated fatty acids).